Anas et al. Biol Res (2020) 53:47 https://doi.org/10.1186/s40659-020-00312-4 Biological Research

REVIEW Open Access Fate of nitrogen in agriculture and environment: agronomic, eco‑physiological and molecular approaches to improve nitrogen use efciency Muhammad Anas1,2, Fen Liao2, Krishan K. Verma2, Muhammad Aqeel Sarwar3, Aamir Mahmood1, Zhong‑Liang Chen2, Qiang Li1, Xu‑Peng Zeng1, Yang Liu4* and Yang‑Rui Li1,2*

Abstract Nitrogen is the main limiting nutrient after carbon, hydrogen and oxygen for photosynthetic process, phyto-hormo‑ nal, proteomic changes and growth-development of plants to complete its lifecycle. Excessive and inefcient use of N fertilizer results in enhanced crop production costs and atmospheric pollution. Atmospheric nitrogen (71%) in the molecular form is not available for the plants. For world’s sustainable food production and atmospheric benefts, there is an urgent need to up-grade nitrogen use efciency in agricultural farming system. The nitrogen use efciency is the product of nitrogen uptake efciency and nitrogen utilization efciency, it varies from 30.2 to 53.2%. Nitrogen losses are too high, due to excess amount, low plant population, poor application methods etc., which can go up to 70% of total available nitrogen. These losses can be minimized up to 15–30% by adopting improved agronomic approaches such as optimal dosage of nitrogen, application of N by using canopy sensors, maintaining plant population, drip fertigation and legume based intercropping. A few transgenic studies have shown improvement in nitrogen uptake and even increase in biomass. Nitrate reductase, nitrite reductase, glutamine synthetase, glutamine oxoglutarate aminotransferase and asparagine synthetase enzyme have a great role in nitrogen metabolism. However, further studies on carbon–nitrogen metabolism and molecular changes at omic levels are required by using “whole genome sequencing technology” to improve nitrogen use efciency. This review focus on nitrogen use efciency that is the major concern of modern days to save economic resources without sacrifcing farm yield as well as safety of global environment, i.e. greenhouse gas emissions, ammonium volatilization and nitrate leaching. Keywords: Nitrogen use efciency, Assimilation, Nitrate, Ammonium, Enzyme, Fertilizer

Introduction Nitrogen (N) plays an important role in crop plants. It is involved in various critical processes, such as growth, leaf area-expansion and biomass-yield production. Excess *Correspondence: [email protected]; [email protected] NUE can support good plant performance and better 2 Key Laboratory of Sugarcane Biotechnology and Genetic Improvement crop out-put. Various plant molecules such as amino (Guangxi), Ministry of Agriculture/Guangxi Key Laboratory of Sugarcane acids, chlorophyll, nucleic acids, ATP and phyto-hor- Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, Guangxi, China mones, that contains nitrogen as a structural part, are 4 Guangxi Crop Genetic Improvement and Biotechnology Laboratory, necessary to complete the biological processes, involving Nanning 530007, China carbon and nitrogen metabolisms, photosynthesis and Full list of author information is available at the end of the article

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protein production [1, 2]. Insufcient amount of N avail- product. Numerous demarcations for NUE have been able to plants can hinder the growth and development. suggested over the years, which have showed a few difer- Nitrogen can also improve root growth, increase the vol- ences in normal ways [4, 25, 26]. ume, area, diameter, total and main root length, dry mass NUE, NUpE and NUtE can be measured by adopting and subsequently increase nutrient uptake and enhance the Eqs. 1, 2 and 3 [4, 24]. nutrient balance and dry mass production [3–6]. NUpE = N contents in plant /N supplied Application of nitrogen increases greenness of plants, (1) CO­ assimilation rate, crop quality-yield and improve 2 = / resistance to environmental stresses such as limited NUtE Yield N contents in plant (2) water availability and saline soil conditions [7, 8]. Hou = × et al. [9] found that nitrogen application more important NUE NUpE NUtE (3) than the other major essential fertilizers/nutrient for suc- cessful crop production. Consequently, N requirement is Nitrogen recovery and agronomic nitrogen ef- the most central feature for plant production [10]. Slow ciency (NRE) are the other common approaches used development of plant and early leaf senescence due to to observe NUE. NRE is termed as the percentage of defcient N can cause decreased both crop production pragmatic nitrogen fertilizer taken up by crop. It is an and quality [11]. Excessive N fertilizer application is com- indicator for a crop to use the N fertilizer that has been mon practice by farmers of cotton regions in the north- supplied [27]. Te yield increment per unit of N ferti- west [12] which is not cost efective for crop production, lizer given to the crop is denoted as agronomic nitrogen and excess N prolongs the vegetative growth period, use efciency (aNUE). It is an important index to meas- delays maturity [13], decrease sugar content, and also ure gain or loss for excess amount of fertilizer [28]. Best attracts insect pest and causes disease epidemics. aNUE is the surety of highest beneft–cost–ratio, which China has only 7% of global farm land with 20% world is a key economic relationship between input and out- population that depends on it for feed [14–16]. It boosts put that relate both by linear curve [29]. up average yield of grain from 1.09 to 6.51 tonnes ­ha−1 Te Eqs. 4 and 5 can be used to measure agronomic in last 7 decades [17]. In China, chemical nitrogen (N) and recovery efciencies like aNUE and NRE: fertilizer input is the major element for the continuous increase of food production to mitigate the problem of aNUE = (Y − Y )/F fertilized not fertilized applied (4) food security [18]. Terefore, the low NUE all over the −1 world especially in agriculture sector is not only wastage Yfertilized and ­Ynot fertilized are yields (kg ha ) when quan- of resources (Fig. 1 a, b) and also problematic for envi- tity of N fertilizer applied was F and zero; ­Fapplied is the ronmental pollution (Fig. 1c, d) and conficting to sus- total N (kg ha−1) applied [28]. tainable agricultural productivity [19–21]. = − NRE (Total NUfertilized Total NUnot fertilized)/N fertilizer dose (5)

NUE and its status Total ­NUfertilized and Total ­NUnot fertilized showed N uptake NUE is an exploiting issue for discussion and research for F and no fertilizer, respectively [30]. which depends on the physiological and metabolic Te variation in NUE can be understood by nitrogen changes, such as soil nitrogen uptake, assimilation from doses, application methods and other agronomic fac- roots to other parts (Fig. 2), source-sink tissues interac- tors which help to manage nitrogen has crucial efect tion for transportation, signaling and regulatory path- for both proftable crop production and environment ways which are responsible for N status within plant and [31]. According to feld demonstrations, Lou et al., [32] growth as well [22]. Normally, the ratio of yield and total measured NRE and aNUE for diferent nitrogen rates, N supplied is termed into NUE [23]. Several techniques application methods and plant population in northwest, have been adopted to observe NUE that can be separated China, and found that the 70% and 80% of nitrogen loss into N uptake efciency and N utilization efciency. N can be minimized when nitrogen applied through drip uptake efciency (NUpE) describes the nitrogen amount fertigation and high plant population, respectively. that a plant can take from sources of nitrogen while N Drip fertigation and high plant density can increase utilization efciency (NUtE) termed as the plant capabil- nitrogen recover efciency for comparable yield. In ity to assimilate plus remobilize N within the plant [4, 22, contrast conventional method of nitrogen application 24]. However, NUE is the resultant of NUpE and NUtE and low plant population, more nitrogen losses, which Anas et al. Biol Res (2020) 53:47 Page 3 of 20

Fig. 1 This diagram depicts country wise (a) and crop wise (b) NUE for 2010 and 2050 (proposed), while c, d shows nitrogen losses in teragram for 2010 and 2050 (proposed)

+ leads to decrease yield in crops due to low amount of in a hydroponic culture containing NH­ 4 -N showed N available. Te midseason rice NUE is less than 30% that the photosynthetic and carbon assimilation rates in China, which indicates that 70% nitrogen is going decreased in the plants [35, 36]. into the ecosystem as loss [33]. As comparison of USA and China from 1980 to 2010 for NUE in case of maize Available sources and forms nitrogen crop, the NUE declined from 30.2 to 29.9 in China but Te conversion of nitrogen from one form to others up-graded from 39.4 to 53.2 in USA [34]. Hajari et al. greatly infuences the nitrogen use efciency.In early − [35] demonstrated few varieties of sugarcane for nitrate growth stage ­NO3 form of nitrogen is important but and ammonium as a source of N fertilizer in their study it has not been commonly used as fertilizers alone, the − and concluded that NO­ 3 -N resulted in higher NUEs other forms go the atmosphere by nitrifcation [37]. How- + as compared to ­NH4 -N. Wheat and maize grown ever, most widely used nitrogen fertilizer urea is abruptly Anas et al. Biol Res (2020) 53:47 Page 4 of 20

increments of mineral nitrogen stock in each soil layer takes place [57, 58]. According to Neto et al. [60] when nitrogen concentra- tion increases even though it is earlier applied, minerali- zation of nitrogen in soil is boosted and a part of N shares from the mineralized nitrogen. Nitrogen within the plants at anthesis stage also enhanced due to the trans- formation of nitrogenous compounds, which have stored nitrogen in earlier growth period [61, 62]. Crop growth, development, biomass and yield have directly linked to nitrogen assimilation [61, 63]. Mazzafera and Goncalves [64] analyzed xylem sap to study nitrogen transformation in cofee plants and found 52% of the total nitrogen is nitrate. But nitrate reductase reduces it into nitrite [65]. Sugarcane accumulates nitrogen 100–150 kg ha−1 in leaves and stalks, only about 55% is removed from stalks up to maturity [66]. Te plant residues after harvesting are put into the feld which gradually mineralized and release N in available forms [67]. Nitrogen consump- tion by enhanced N fertilization to the crop may lead to high N uptake but it is not necessary to increase biomass production [68]. Tus, over use of nitrogen fertilizer down-regulates the nitrogen use efciency and increases production cost and environmental pollution. − Plants have the ability to acquire excessive NO­ 3 nitro- Fig. 2 The major plant pats which have their own role for NUE. a gen than the requirement for assimilation and store it in Grain: responsive to fertilizers and nutrient storage component, b unassimilated pools like vacuoles of leaves [69], become Shoot: nutrient redistribution, assimilation and transportation (source available for utilization under low N [70, 71]. Hajari and sink), c Roots: Efcient nutrients uptake by transporters and et al. [35] and Robinson et al. [37] found, the ­NO −-N channels 3 per gram was higher in dry roots than the shoot on all growing media. Hajari et al. [35] claimed that the sug- − arcane plant is not able to translocate ­NO3 -N from nitrifed (Fig. 4) after conversion to ammonium [37]. root to shoot efciently due to which limited N uptake Although urea after application in soil can convert into and transport occur rather than assimilation which may nitrate and ammonium form, it is not still clear about afect the NUE in sugarcane. Te application of a nutri- urea uptake process and metabolic changes in plants [38]. ent may increase (synergism) or decrease (antagonism) Urea is also preferred and predominant source of N due the contribution of the other nutrients in crop yield. Te to more nitrogen contents and low cost to produce it in concentration of phosphorus and nitrogen varies over the South Africa [39]. growing period in the soil and create interaction either Te soil N (Fig. 3) is most important to observe the ef- synergistic or antagonistic. Te response of crop yield ciency of N in the agricultural feld conditions [40–44]. might be afected directly or indirectly [72, 73]. Tere- Tere are a lot of evidence from various feld trials using fore, the supply of both N and P creat changes in chemi- 15N-labeled fertilizer, N uptake is principally derived cal, physical, and biological properties of soil [74, 75]. Te from soil (Fig. 3) rather than fertilizer [45–53]. How- nitrogen fertilizer has synergetic efect to phosphorus. ever, many studies have been conducted and found that Te results indicated, addition of nitrogen along with unfertilized N responses often give more yield than that phosphorus fertilizer produced better positive interac- of N fertilized [43, 54–56], except those in which soil tion than separately [76]. In the sugarcane feld which has N availability is captured by accumulation of carbona- previously wild vegetation and low available phosphorus ceous residues. Total soil nitrogen and organic carbon response nutrient limitations, it involves phosphorus as vary in soil profle, both decreases with the soil depth, limiting source in high demand periods, and also micro- + − − bial biomass [77–85]. however the ionic forms of N (NH­ 4 , ­NO2 , and NO­ 3 ) shape the mineral nitrogen dynamics because discrepant Anas et al. Biol Res (2020) 53:47 Page 5 of 20

Fig. 3 Sources of organic nitrogen available for mineralization in soil [59]

Losses of nitrogen in the ecosystem in fertilizer applications in China was noted, and it con- Worldwide high nitrogen fertilizer application results in sumed 30% of total N fertilizers synthesized around economic loss and ecological hazardous due to extra con- the world in 2002, in spite of the facts, its arable land sumption of resources, water eutrophication, and high accounts only 10% of the world aggregate. However, the rate of greenhouse gas emissions along with potential use of vast amounts of synthetic N fertilizer to expand leaching. Te inefcient N utilization with poor transfor- crop yield are not fnancially sustainable and put a sub- mation of provided N results in unintentional fertilizer stantial burden on farmers, and furthermore result in loss in soil, atmosphere and promoting contamination environmental pollution. Every crop cannot use about of groundwater, distort connecting biological communi- 50% nitrogen fertilizer during its growing season due ties and cause dangerous atmospheric deviation, through to over fertilization [90].Moreover, plants grown under the emission of the poisonous ozone depleting substance excessive nitrogen applications are more susceptible to nitrous oxide [82], eutrophication, air pollution, N leach- lodging because of shoot overgrowth and tender, and ing, water pollution, soil acidifcation and soil degrada- pest damage and disease, and also degrade quality of the tion [14, 18, 82–89] which is not suitable for environment grains [91]. friendly crop production and human life (Fig. 4). Te N losses thru lixiviation, direct escape to the air, In agriculture, crop production requires plentiful N denitrifcation and/or percolation is higher due to over which is the most widely recognized limiting factor for use of N fertilizer [92]. Te synchronized application crop growth, development and yield. A lot of synthetic as the demand of plant at its critical stage can decrease N fertilizer is applied to arable land by growers to fulfll losses of applied N fertilizer [93–95]. Over the last dec- the demand for crop production. An abrupt increment ade, crop response to N fertilization [96, 97] was detected Anas et al. Biol Res (2020) 53:47 Page 6 of 20

Fig. 4 Summary of nitrogen sources and, their conversion, availability to plants and losses within/outside of soil

in sugarcane felds all over the Brazil for green cane trash has signifcant contribution to pollute environment in blanketing systems (GCTBS) and also in situ quantify Australia [115]. Many researchers in Brazil also fnd out ­NH3 volatilization [98], ­NO3 leaching [99–101], and N­ 2O leaching losses of nitrogen in planted sugarcane through- emissions [102, 103], N use efciency [104, 105]. About out its growth [116]. However, during ratoon season, − 60–80% synthetic N fertilizer is not taken up by sugar- NO­ 3 leaching is more important than the planted cane cane crop under GCTBS, and losses due to volatilization, [100]. Te skips within ratoon sugarcane feld increased denitrifcation and leaching has been observed, but most across the growth period, and decreased the crop N of the mineral N is not available for micro biota, while response. Te unique response to applied N fertilizer can the remaining part available to the crop [96]. In spite of be attained by well-established ratoon crop similar to the fact that the mechanism of commercial fertilizers is planted crop density. relatively well familiar [106]. However, many research- Duan et al. [117] discuss their fndings about N appli- ers claim the impact of organic and organomineral is cation to long and short vines of sweet potato, the both not understood on chemical and microbial properties long-vine and short-vine cultivars have the peak yield for of soil for successful crop cultivation in temperate areas nitrogen applied as 30 and 90 kg ha−1 respectively. Te [107–109]. cultivars of same production potential have reduced their Biotic factors like size and diversity of microbial com- yields, and the root yield of long vine is signifcantly lower munity and abiotic factors temperature, soil moisture than that of short vine for nitrogen 120 kg ha−1. Wu et al. content, temperature have direct relation to regulate [118] also claim the cultivar Zijing No. 2 decrease in the organic compounds mineralization in the soil (Fig. 3), root yield for N application (75 kg ha−1) in fertile soil. however, seasonal climatic change during cropping sea- Tus, the genotypic diferences in sweet potato have a son fuctuate the mineral N availability [110]. Rapid avail- great infuence on the partitioning of dry matter as well ability of mineral N in soil solution has been noted as a as uptake of nitrogen [119]. Wilson [120] classifed culti- result of synthetic N fertilizer application [96, 111, 112], vars of sweet potato for N-responsiveness, nonresponsive but there is a powerful race between crop plants and and depressive natures. Nitrogen buildup and distribu- + micro fora for existing mineral N (especially ­NH4 ), and tion for short stature tuber roots are greater, and simi- cause a large variations over time [77, 78]. larly exhibit more yield in response to high N conditions Urea is the major N fertilizer that is applied to the feld [121]. Besides, the cultivars that require higher N, give and also the main source of ­NH3 gas emission (Fig. 4) higher root yield in fertile soils [118]. from agronomic practices [113] contributing for about Total nitrogen fertilizer can be reduced up to 20% of the emissions in Germany [114] and is highly 360 kg ha−1 with respect to 430 kg ha−1 for cropping important in many other countries like China. Nitro- system based on the wheat–maize rotations, along − gen loss as NO­ 3 leaching (Fig. 4) from sugarcane feld with improved agronomic practices. It was resulted in Anas et al. Biol Res (2020) 53:47 Page 7 of 20

increase in maize yield by 7–14%, but reduction in wheat rate by integration management practices [140]. Te yield, ­N2O and NO emissions by 1–2%, 7% and 29%, reports from diferent regions/countries suggest that N respectively [122]. In addition, best fertilization practices use efciency can increased by decreasing N application are an option to improve NUE and also seasonal collec- rate [141–144]. However, it also depends on agronomic tive ­N2O emission decrease [123]. Leaching process can traits, fertility of soil, management and yield potential be minimized by adopting legume crops in cropping [141–144]. system up to 50% than the conservative systems [124]. Te N application rate can also be determined by veg- Soybean reduces 50–60% of N demand by biological etative growth and productivity index, for example, cof- nitrogen fxation [125]. Graham et al. [126] and Resende fee plants showed high rates for it between 2400 and et al. [127] observed that addition of synthetic fertilizers 3600 kg ha−1 per year [60, 145] and N as urea applied decreased soil N stocks, while Ladha et al. [108] reported 600 to 800 kg ha−1 to maintain this productivity in Bra- an increase in soil C pool and N stocks for long–term zil. Ofcial recommendations for nitrogen fertilizer are organic fertilizer application. 400 kg ha−1 ­year−1 [61] and apply in tow or four splits. But the cofee growers applied urea between 600 and 800 kg ha−1 in 26 splits during cofee cycle. In fact, they Agronomic and physiological approaches attempted this practice to stop N defciency, but causing Application rates low nitrogen use efciency [146]. Luo et al. [32] suggests Irrational application of nitrogen is a major problem of that 20% N can be reduced, when plant density is high, low nitrogen use efciency [128–130]. Terefore, agro- without yield loss and also can reduce for drip fertigation. nomic principles and practices should utilized in mod- ern techniques to enhance nitrogen use efciency, so as Application methods the reduced application rate of fertilizer inputs without Te international plant nutrition institute is convincing yield reduction is key factor [32]. Soil characteristics the best agronomic practices, 4R nutrient application and agro-climatic conditions highly force the applica- principles, i.e. source of fertilizer, rate, time and site/place tion level of fertilizer [131]. Crops can use only up to 35% [147]. Soil fertility varies with in the feld abruptly which of the supplied N during its complete life cycle [39] and has strong impact on yield and nutrient uptake by culti- the remaining is escaped to the environment by various vated crops, and this major problem can be handled by mechanisms and functions (Fig. 4) [132, 133]. adopting site-specifc nitrogen fertilization. Site-specifc Improvements in NUE by decreasing nitrogen dose N fertilization provides signifcant impacts in terms of may delay leaf senescence which results in no yield loss. economy and ecology in heterogeneous felds [148–150] Late-season leaf senescence due to low nitrogen applica- which results in enhanced yield, quality and ultimately tion rate provides relatively higher photosynthetic capac- high nitrogen use efciency. ity to crop and ultimately increase yield production. Spectral measurement is a suitable approach to know Mulvaney et al. [109] proposed N mineralization in soil is the nitrogen requirements of crops and site-specifc positively regulated by synthetic nitrogen fertilizer. Tese application for precise farming [151]. Te principle fndings indicate that N may exceeds the demand of sug- behind laser-induced chlorophyll fuorescence (LICF) −1 −1 arcane crop (200 kg ha ­year ) and afect C:N ratio in is used to the measure the N situation of the crop stand soil for long time continuous applications. by close distance [152] as well as 3–4 m [153]. Te plant Srivastava and Suarez [134] confrmed N recommen- nitrogen is measured indirectly by chlorophyll content dation rate for sugarcane varies worldwide for 45 to via fuorescence signals ratio at 690 and 730 nm [154, −1 −1 300 kg ha but 60 to 140 kg ha is recommended for 155]. It indicates that high amount of chlorophyll resulted Brazil. Dametie and Fantaye [135] summarised the results in lower fuorescence radiation ratio F690/F730 because of sugarcane N uptake studies by various researchers in reabsorbed radiations have more strength at 690 nm. the globe, and indicated that the usual need of ratoon Rubisco acts as the sink of N and has close relation to −1 crop for nitrogen is 1.5 kg Mg cane yield. N uptake chlorophyll content, thus the ratio F690/F730 describes −1 varied from 0.88 to 1.47 kg Mg in Hawaii, and stubble the N content of the plant [156]. −1 cane production required 1.3 kg Mg [136, 137]. By the Crop canopy sensor calibration is too sensitive to feld compilation of numerous results for nitrogen dosage and variability like the ramp calibration strip [157] or the technically recommendations in Brazil, the usual rate is calibration plot methods [158]. Te reference area for −1 1.0–1.4 kg Mg cane [138]. canopy sensor within a feld should be given according Nitrogen fertilizer application dose can be minimized to feld and soil variability [159] that also relates to the by 20% without yield loss in Australia [139]. Te N fer- sugarcane plant density variation. Te calibration should tilizer in China has possibility to use moderately at low be done for every crop and season, separately [160]. Yong Anas et al. Biol Res (2020) 53:47 Page 8 of 20

et al. [161] applied nitrogen fertilizer at various concen- Drip fertigation trations among the rows of maize-soybean relay inter- Northwestern China has an arid climate, cotton produc- cropped feld at three diferent distances (15 cm, 30 cm tion in this region is not possible without irrigation and and 45 cm) and concluded that crop performed better for N fertilization [171]. Drip fertigation is a good option to 15 cm and 30 cm treatments. Te NUE and total grain supply water and fertilizers in precise quantities [172, yield of the maize-soybean relay intercropping system 173]. Drip fertigation with mulching is going to be exten- were signifcantly higher in 15 cm and 30 cm. So, lower N sively used in recent years [174]. It is well documented application at 15–30 cm from fertilizer application loca- that the nutrient and water use efciency both can be tion to the maize row was optimal. enhanced through drip fertigation that improves crop Productivity of low land rice has a great dependence production for each unit of nutrients and water [172, on the selection of varieties and their nutrient utiliza- 175]. It has more advantage of the soluble fertilizers that tion capacity. Under dose of N fertilizer may happen, can be put in specifc quantity alongside the good crop especially when N is subject to immobilization follow- health and potential yield because of maintained fer- ing ratoon crop fertilization for unburned sites [56]. tigation in the root zone [173]. Many studies pointed Crop response to inputs is also infuenced by climate, out fertigation can improve fertilizer use efciency by for example, high altitude of Andhra Pradesh is endowed decreasing application rates without losing crop yield with the special soil and climate where varietal responses [176, 177] and especially drip fertigation of cotton feld to inputs vary relatively to coastal plains. Diferent nitro- with reduced nitrogen, improved its efciency [175, 178]. gen sources should be jointly applied to fulfll the require- It improved cotton yield, yield components, and leaf area ment of nitrogen to improve crop productivity [162]. index (LAI) by 20 to 30% as compared to furrow irriga- Te supply of N fertilizer to sugarcane is afected by soil tion [179]. However, maximum nitrogen recovery was profles that are hard to measure inside the agricultural obtained by sacrifcing cotton yield at lower N level land [53]. Indeed, even the selection of reference regions, under drip fertigation [180]. So, an optimum N level for that get satisfactory measures for nitrogen, according to drip fertigation has important role to achieve highest cot- Raun et al. [163], can be risky with regards to evaluat- ton yield. ing sugarcane N feedback; depending upon where refer- Traditional high nitrogen application without consid- ence zones were set up, the harvest N reaction can difer ering method of application and plant population gives altogether. For instance, producers may realize that a more seed cotton yield. Anyhow, N can be reduced up yield did or did not respond to N application,and such to 15–30% when drip fertigation is employed and 20% conficting results found in various experiments were in case of high plant population without sacrifcing seed demonstrated by Duan et al. [117]. Hence, use of can- cotton yield. Te fndings of Luo et al. [32] are that N opy sensors to quantify the N response is troublesome reduction up to 30% has non-signifcant seedcotton yield because of variable plant density inside the felds. In that reduction for drip fertigation. However, drip fertigation capacity, diferent elements can veil the N impacts, like shows increase by 5 and 20.7% in seedcotton yield for 15 soil compaction, pest attack and diseases. Zillmann et al. and 30% nitrogen reduction. [164] announced a comparative issue when they con- In other words, drip fertigation with high plant popu- ducted a test for N connected to maize. For all the experi- lation is an important attribute to save nitrogen with mental area, the crop response for N was not similar as sustainable yield for arid culture. Many experiments proposed. have conducted to fnd agronomic practices, high plant- Te canopy sensor has to be utilized when the sugar- ing density, diversifed planting geometry [181] organic cane tallness is between 40 and 70 cm to get estimation fertilizers and improvement of application method of afectability to sugarcane vigor fuctuation [165, 166]. At nutrients are helpful to regulate cotton yield for reduced this stage, sugarcane has attained around 10–30% of total nitrogen conditions in the Yellow River valley, China [11, biomass with 27–68% N, which is dependent on geno- 12, 140]. type, soil fertility, climate and developmental stage [167]. N requirement of crop prior to treatment can achieved N and plant density by various sources, i.e. mineralization of organic sources Te plant density is an important tool to testify N rate and endophytic nitrogen fxation by bacteria related to without sacrifce of yield either by increase or decrease plant roots [53, 168–170], and also other inputs to the in number of plants per unit area [12, 140, 182]. It var- feld like vinasse, poultry manure and farmyard manure ies active crop canopy refectance on the base of ground etc. for sensors [183]. Tis idea has been profciently utilized to control N application for rice [121], maize [184–188], cotton [189] and wheat [188, 190, 191]. Te application of Anas et al. Biol Res (2020) 53:47 Page 9 of 20

nitrogen based on canopy sensor depends on chlorophyll occupies largest planting area in Southwest China that is of crop canopy which describes nitrogen status [192], helpful to improve nitrogen, light use efciencies and soil but it is not as valid for sugarcane. Te feld-scale sensor nutrient availability [20, 199–204]. observations at the leaf level poorly show a relationship Tere are many previous studies indicating that high with nitrogen and chlorophyll status [166]. It is due to N input has undesirable outcome for biological nitrogen irregular sugarcane canopy which may show ground soil fxation [205]. When nitrogen availability studied for leg- to the sensor. Dynamic and manually monitored canopy ume-nonlegume mixtures, high content of mineral nitro- refectance sensors are available, which consider all the gen in soil triggers the microbial nitrogen fxation and parameters for sugarcane biomass variation, principally hence availability of nitrogen decrease for nonlegume efected by plant population, as described by Amaral crop [206]. However, low input of nitrogen increased et al. [138]. signifcantly fxation and stimulated the translocation of Amaral et al. [138] conducted strip experiments for fxed N to nonlegume [203, 207]. diferent nitrogen rates and validated that the uniform distribution of canopy has no trouble for canopy sensor. NUE regulating enzymes and genes Variation in the canopy is mainly afected by plant popu- Te major sources of nitrogen, taken up by higher lation and vigor rather than the nitrogen supply. Six trials plants, are nitrate and ammonium as synthetic fertiliz- with difering nitrogen supply were conducted at difer- ers, organic compounds and amino acids etc. It depends ent locations, fve out of six trials has non-signifcant upon the availability of nitrogen, and within the plants response to variable nitrogen supply and the sixth trial it is controlled by many metabolic pathways and genes may have variation in soil characters, deeper root zone expression levels [208]. Nitrogen use efciency is depend- and more water holding capacity, therefore increases soil ent of soil nitrogen conditions, photo synthetically fxed nutrient utilization and crop vigor. carbon dioxide to provide precursor for biosynthesis of many amino acids and vice versa [209, 210]. It has been Intercropping also claimed that all the inorganic nitrogenous fertiliz- Intercropped crops are signifcantly infuenced by fer- ers frst converted to ammonium before uptake by higher tilization methods and show better growth for diverse plants [211]. Nitrate reduction occurs in roots as well as nitrogen supply for interspecifc rows instead of intraspe- shoots but nitrate reduced directly in cytoplasm while in cifc [193]. Interspecifc applications accelerate resource plastids/chloroplast via nitrite [208]. Reduction of nitrate use efciency, soil productivity and also have posi- to nitrite occurs in cytosol by nitrate reductase enzyme tive impacts on the environment [194–197]. Tis sys- (Table 1) [212]. Nitrite is transported into chloroplasts tem involves more than one crop in a season, and can in leaves where nitrite is converted to ammonium ions be observed in the Huang Huai Hai, China [198], and due to nitrite reductase (Table 1) [213]. Te products relay intercropping system is common in the Southwest of ammonia, glutamine and glutamate, act as donor of China where one crop or three crops in 2 years are grown the nitrogen during biosynthesis for nucleic acid, chlo- [199]. So, better nitrogen fertilization methods and relay rophyll and amino acids. Te isoenzymes of glutamine or intercropping systems based on soybean (legume synthetase, glutamate synthase, and glutamate dehydro- crop) greatly infuenced on soybean yield with decreas- genase (Table 1) have been proposed for three major ing environmental cost. But environmental features like ammonium assimilation processes: primary nitrogen rainfall, light intensity and heat can be limiting factors assimilation, reassimilation of photorespiratory ammo- for cropping systems. Maize-soybean relay intercropping nia, and “recycled” nitrogen [213]. Organic nitrogen in

Table 1 The basic information of enzymes involved in nitrogen metabolism of plants Enzyme Abbreviation Encoding genes Function

Nitrate reductase NR 5 Reduce nitrate ion into nitrite ion Nitrite reductase NiR 30 Further reduce nitrite into ammonium ion Glutamine synthetase GS 49 Involve in GOGAT pathway Glutamine oxoglutarate aminotransferase GOGAT​ 15 Involve in GOGAT pathway Glutamate dehydrogenase GDH 3 Dehydrogenate α-ketoglutarate Aspartate aminotransferase AST 13 Catabolise glutamate into aspartate Asparagine synthetase AS 4 Aspartate is converted into asparagine Anas et al. Biol Res (2020) 53:47 Page 10 of 20

the form of amino acids transferred from source organs Each monomer of homodimer nitrate reductase asso- to sink (Fig. 2), for example, glutamine and glutamate ciated with three prosthetic groups: favin adenine can be used to form aspartate and asparagine [211, 214]. dinucleotide (FAD), a molybdenum cofactor (MoCo) Te ammonium nitrogen is transferred into amino acids and a haem. NR reduces chlorate into toxic chlorite, by the enzymes e.g. glutamine synthetase, glutamate responsible gene for that in mutant has been identi- synthase, asparagine synthetase and aspartate amino fed, the Nia genes encoding the NR apoenzyme and transferase (Table 1). Te coherent situation existed for the Cnx genes encoding the MoCo cofactor. [208, 222]. glutamate dehydrogenase either it is involved in assimila- Te Nii genes have one to two copies encoding the NiR tion of ammonium nitrogen or carbon cycling [215, 216]. enzyme [208]. GS having decameric structure is con- Te ammonium assimilating enzymes are important trolled by two classes of genes, GLN1 and GLN2, [223]. during grain flling stage due to its remobilization. Te GLN2 (single nuclear gene) encodes chloroplastic GS2, biosynthesis of amino acids from ammonia is occurred involved in ammonium assimilation or re-assimilation by the GS and GOGAT pathways (Fig. 5) [217]. Nitro- either from nitrate reduction in ­C3 and ­C4 plants or gen reutilization is an important phenomenon involving photorespiratory product of C­ 3 plants [224]. On the NADH-GOGAT enzyme, rice grain weight increased other hand, GS1 isoform is encoded by GLN1 gene up to 80% due to over production of NADH-GOGAT family which recycles ammonium during leaf senesc- [218]. Glutamine dehydrogenase involves for senescing of ing and transport in the phloem sap [225]. Vanoni leaves and also controversy as deaminating (Fig. 5) [219, et al. [226] reported that GOGAT (mechanistic struc- 220] and aminating directions [23]. Young leaves recycle ture) has two forms Fd GOGAT (in leaf chloroplast) nitrogen from chloroplast by GS2 and Fd-GOGAT. In and NADH GOGAT (in plastids of non-photosynthetic GOGAT catalyzed proteolysis, GS2 and de facto NiR are tissues). Tree genes (ASN1, ASN2 and ASN3) encode responsible for breakdown of chloroplast during senes- asparagine synthase, and substrate ammonia is utilized cence. Production of glutamine during leaf senescence is by asparagine synthase to form asparagine [227]. Stor- basically dependent on GS1 isoform. Substrates for GDH age compounds, long-range transporter and glutamine are produced from chloroplast proteins proteolysis, and has lower N/C ratio than asparagine [228, 229]. In plas- deaminating activity provides 2-oxoglutarate and ammo- tids; bicarbonate, adenosine tri-phosphate and amide/ nia. Glutamine for new sink organ is produced by GS1 ammonium from glutamine act as substrate for car- reassimilation of ammonia [221]. bamoylphosphate synthase (CPSase) to form precur- sor (carbamoylphosphate) of citrulline and arginine.

Fig. 5 Schematic diagram to show the fate of nitrogen within the plant Bolded NO−3 and NH+4 are nitrogen uptake forms by roots through diferent transporters Anas et al. Biol Res (2020) 53:47 Page 11 of 20

Te subunits (small and large) of carbamoylphosphate In conclusion, GS activity has direct relation with bio- synthase (CPSase) encoded by car A and B genes, mass or yield in transgenic plants [254]. Over-expression respectively [230]. Finally, glutamate is produced by of NADH-GOGAT increased in grain yield for transgenic mitochondrial NADH-glutamate dehydrogenase for rice plant [231]. So, it is important to know the alleles of higher levels of ammonium [23]. genes and promoters to improve yield by overexpressing GS or GOGAT genes. Overexpressed ASN1 in Arabidop- NUE responsive genes manipulation sis increased soluble protein content in seed, total pro- Crop varieties that are highly N efcient, high yields tein and plants ability to grow for limited nitrogen supply with reduced N input is the main solution for improv- [229]. Tese results suggested that NUE can be improved ing NUE [231–233]. Recent studies documented that by manipulating downstream steps in N-remobilization. shoot-to-root signaling pathways, feedback mechanisms Further studies of carbon metabolism pathways also have and amino acids transportation in roots and shoots potential to improve NUE [255–257]. infuence the nitrogen uptake and its metabolism [234– Several external and endogenous factors infuenced 238]. With the aim of improving NUE, approaches have the expression of genes which are highly regulated at the been adopted on the basis of genetic changes for nitro- transcriptional as well as post-translational levels [208]. gen uptake [239–241], nitrate allocation [242], nitrogen Lea et al. [218] demonstrated that post-translational reg- metabolism [218, 243–249] and the regulation [250]. ulation afects the amino acids, ammonium, and nitrate Many critical candidate genes also have been over- levels, whereas transcriptional regulation has only minor expressed and knocked out in order to test for biomass infuence. Plants unregulated for NR accumulate high and plant nitrogen status. Nitrate infux increased due concentrations of asparagine and glutamine in leaves. to over-expression of HATS-like NRT2.1 but at the same Tus further characterization can provide the useful time NUE and its utilization phenotypically remains properties for crops. unchanged [46]. Overexpression of genes encoding for Asparagine synthetase (AS) encoded by a small gene NR/NiR in transgenic plants to improve NUE has no family, catalyzes the formation of asparagine (Asn) surety for its utility. Nitrate reductase related gene over- (Fig. 5) and glutamate from glutamine (Gln) and aspar- expression in tobacco plants showed delayed NR-activity tate [258]. Te role of AS and GS interaction in primary for drought conditions and quick recovery for re-water- N metabolism is very crucial [259, 260]. GS negatively ing after short time drought [251]. It has been observed correlates with the AS transcript levels and polypeptides that nitrate level decreased in transgenic Arabidopsis, in the transgenic plants suggesting that AS showed com- tobacco and potato plants without improving in biomass, pensation for GS ammonium assimilatory activity [260, number of tubers and seeds respectively. Regardless of 261]. It is hypothized that AS might be important in reg- the nitrogen available sources, Nia or Nii genes overex- ulation of the reduced N fux into plants due to decreased pression improved mRNA levels besides N uptake afect GS activity. However, the GS is essential to synthesize without any change in the yield and growth, indicat- Gln for biosynthesis of Asp via NADH-GOGAT and ing the composite post-transcriptional regulation of NR AspAT [260]. Lam et al. [229] demonstrated the results of [252]. overexpressed the ASN1 gene in Arabidopsis as enhanced When we talk about GS1 and GS2 genes expression, soluble seed protein content, total protein content with the overexpressed GS2 has been testifed along with better growth on N-limiting medium. However, in case Rubisco promoter in Nicotiana tabaccum and CaMV 35S of ASN2 gene endogenous ammonium accumulation was promoter in Oryza sativa [4, 217]. It enhanced growth less compared to wild-type plants as growing on 50-mM rate in Nicotiana tabaccum and photorespiration and ammonium medium [22]. Signaling processes are attrac- drought tolerance in Oryza sativa. Overexpression of tive clues for metabolic engineering. Physiological activ- GS1 genes with promoters having diferent combina- ity of glutamate dehydrogenase (GDH) is still unclear as tions, RolD, CaMV 35S and Rubisco subunit (rbcS) have compared to GS/GOGAT enzymes [215]. Ameziane et al. been reported with positive results for plant biomass [241] investigated GDH activity in transgenic tobacco and grain yield. For example, grain yield and roots are plant, and the biomass production increased in gdhA signifcantly higher with more N content in nitrogen transgenic plants without considering growing condi- efcient wheat lines under the control of the rbcS pro- tions either controlled conditions or feld. moter observed [248]. Similarly, biomass and leaf protein in Nicotiana tabacum (over expressed GS1) increased Microarray and whole genome sequencing under the control of CaMV 35S promoter [253]. Another It has been observed that N uptake remains constant overexpression of GS1 gene depicted 30% increase in throughout domestication of extraordinary maize vari- yield of maize due to more kernel number and size [231]. eties but utilization of N enhanced, which support the Anas et al. Biol Res (2020) 53:47 Page 12 of 20

hypothesis of conventional breeding programs improv- emerging technology for all plants [265, 266]. Molecular ing NRE capacity [262]. Interestingly, inconsistency of and physiological techniques have been employed in last overexpressed key enzymes (NR, NiR, GS, and GOGAT) two decades to know the diferentially expressed genes for an improvement of NUE or phenotypic change is also (DEGs) in Oryza sativa [267, 268], Sorghom bicolor [269], a challenge [218, 231, 254, 262]. Due to these reasons, Glycin max [270] and Camilia sinensis [271] for low new molecular techniques like microarray and transcrip- nitrogen levels. Past studies mostly relied on single geno- tome (Fig. 6) are consider as emerging tools to study the type for genes expression all over the world for low and response of plants whole genome. normal nitrogen conditions either for nitrate or ammo- Te arrangement of known and unknown DNA sam- nium [267–271]. However, two genotypes of Camilia ples on a solid support is known as microarray. Every sinensis were studied and compared for both levels of microarray contains thousands of spots, each has less nitrogen in ammonium form. Genotypic contrast for than 200 µM diameter and called probe [263]. Tese global genes expression and comparative analysis helped arrays may be in diferent formats and also probes to compact the knowledge of candidate genes for NUE. can be smaller as oligonucleotides, cDNA or genomic A lot of information in literature regarding quantita- sequences. Diferent techniques (photolithographic, nib, tive trait loci (QTLs) responding NUE are also available pin or inkjet) are employed to format. Te probes are [272–274]. Te combination of DEGs and QTLs datasets labelled radioactively or fuorescently and hybridization has great importance to develop new nitrogen use ef- controlled electronically [264]. cient genotypes in future [275]. Whole genome sequencing is a modern approach to Recent next generation sequencing technologies for understand the changes at genomic level, expression level transcriptomic profling are helpful to understand the of genes and specifc genes related to the desired traits. genes transcription and regulation of transcripts at all Good quality genome sequence information of ideotype levels [276]. Illumina’s RNA-sequencing platform was rice and Arabidopsis plants are available for microar- used for transcriptomic exploration of genes expres- ray analysis, but the transcriptomic profling (Fig. 6) sion to investigate the response of nitrogen nutritional for whole genome sequencing of RNA is an excellent stress in plants. It has been reported that the amino

Fig. 6 Work fow chart for transcriptomic profling for crops Anas et al. Biol Res (2020) 53:47 Page 13 of 20

acid transporters in wheat plants play important role to (2020) and Fund of Guangxi Academy of Agricultural Sciences (2015YT02). The funding bodies played no role in the design, execution, interpretation of the transport nitrogen for development and a biotic stress data, or writing of the manuscript. conditions [277]. Based on the transcriptomic profling Dai et al. studied the regulatory mechanism for storage Availability of data and materials Not applicable. protein in wheat grain in response to nitrogen supply during grain development [278]. Asparagine has crucial Ethics approval and consent to participate importance for nitrogen uptake in roots and considered All applicable international, national, and/or institutional guidelines were followed. as ideal nitrogen transporting molecule [258, 279, 280]. According to Curci et al. genes encoding asparagine Consent for publication were down regulated in leaves and roots of durum wheat All authors of this paper consent for publishing manuscript and fgures in this journal. under limited nitrogen [276]. It has been clearly observed that genes were down regulated in roots and leaves which Competing interests were involved in carbon, nitrogen, amino acid metabo- All authors declared no confict of interest. lisms, and photosynthetic activity for plants grown under Author details nitrogen free conditions [268]. 1 College of Agriculture, Guangxi University, Nanning 530005, China. 2 Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture/Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Conclusion Sciences, Nanning 530007, Guangxi, China. 3 Crop Sciences Institute, National Agricultural Research Centre, Islamabad, Pakistan. 4 Guangxi Crop Genetic Te agronomic and molecular approaches altogether Improvement and Biotechnology Laboratory, Nanning 530007, China. have potential to improve nitrogen use efciency. Nitro- gen losses can be minimized by precision agriculture, Received: 17 December 2019 Accepted: 20 September 2020 cut of nitrogen dose, intercropping of legume and non- legume crops, improving plant populations and introduc- ing nitrogen efcient genotypes. Although the studies have been conducted to improve nitrogen use efciency References 1. Frink CR, Waggoner PE, Ausubel JH. Nitrogen fertilizer: retrospect and of many crops by manipulating single or more genes prospect. Proc Natl Acad Sci. 1999;96:1175–80. but now the advanced technologies like whole genome 2. Crawford NM, Forde BG. Molecular and developmental biology of sequencing are more important for future studies. inorganic nitrogen nutrition. Arabidopsis Book. 2002;1:e1. 3. Stitt M, Krapp A. The interaction between elevated carbon dioxide and Molecular breeding instead of conventional breeding is nitrogen nutrition: the physiological and molecular background. 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